Rh glycoprotein expression is modulated in pufferfish (<i>Takifugu rubripes</i>) during high environmental ammonia exposure

Nawata, C. Michele; Hirose, Shigehisa; Nakada, Tsutomu; Wood, Chris M.; Kato, Akira

doi:10.1242/jeb.044719

Cited by 97 publications

(16 citation statements)

References 74 publications

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“…Interestingly, NH 3 excretion was significantly increased at the onset of elevated CO 2 relative to control values. This is consistent with the ammonia trapping theory in which apical NHE function facilitates NH 3 excretion454647.…”

Section: Discussionsupporting

confidence: 91%

Carbon dioxide induced plasticity of branchial acid-base pathways in an estuarine teleost

Allmon¹,

Esbaugh²

2017

Sci Rep

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Anthropogenic CO2 is expected to drive ocean pCO2 above 1,000 μatm by 2100 – inducing respiratory acidosis in fish that must be corrected through branchial ion transport. This study examined the time course and plasticity of branchial metabolic compensation in response to varying levels of CO2 in an estuarine fish, the red drum, which regularly encounters elevated CO2 and may therefore have intrinsic resilience. Under control conditions fish exhibited net base excretion; however, CO2 exposure resulted in a dose dependent increase in acid excretion during the initial 2 h. This returned to baseline levels during the second 2 h interval for exposures up to 5,000 μatm, but remained elevated for exposures above 15,000 μatm. Plasticity was assessed via gene expression in three CO2 treatments: environmentally realistic 1,000 and 6,000 μatm exposures, and a proof-of-principle 30,000 μatm exposure. Few differences were observed at 1,000 or 6,000 μatm; however, 30,000 μatm stimulated widespread up-regulation. Translocation of V-type ATPase after 1 h of exposure to 30,000 μatm was also assessed; however, no evidence of translocation was found. These results indicate that red drum can quickly compensate to environmentally relevant acid-base disturbances using baseline cellular machinery, yet are capable of plasticity in response to extreme acid-base challenges.

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Section: Discussionsupporting

confidence: 91%

Carbon dioxide induced plasticity of branchial acid-base pathways in an estuarine teleost

Allmon¹,

Esbaugh²

2017

Sci Rep

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“…This indicates that the acid–base regulatory machinery of squid early life stages responds to increased environmental hypercapnia by potentially increasing acid–base regulatory capacities. Although information from exclusively marine organisms is still scarce, few studies investigated the role of acid and ammonia extrusion mechanisms in euryhaline teleosts and crustaceans in response to elevated environmental p CO 2 or ammonia concentrations [24,25,57-59]. Recently, a full length sequence for RhP from dungeness crab Metacarcinus magister was cloned and tested for transcript abundance during acclimation to elevated environmental ammonia levels [57].…”

Section: Discussionmentioning

confidence: 99%

“…In teleosts one type of ionocyte, the so called proton pump rich (HR) cells, which express V-type H + -ATPase (VHA), Na + /H + exchangers (NHE), Rh glycoprotein c (Rhcg) and Na + /K + -ATPase (NKA), are believed to be specialized in the secretion of acid equivalents [20]. It is proposed that ammonia transporters from the Rh family in combination with NHE3, expressed in HR cells are key players in mediating the active secretion of ammonia and protons in seawater teleosts [23,24]. …”

Section: Introductionmentioning

confidence: 99%

“…Generally, information regarding the molecular characteristics and functionality of Rh proteins is very limited for marine invertebrates although many of them are ammonoteles, relying on efficient ammonia excretion pathways [25]. Rh proteins are of particular interest in the context of CO 2 -induced acid–base disturbances as they were proposed to have dual NH 3 /CO 2 transport function [24,26,27]. Thus, Rh proteins may represent key players of acid–base regulation and gas exchange during environmental hypercapnia by facilitating CO 2 diffusion.…”

Section: Introductionmentioning

confidence: 99%

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Development in a naturally acidified environment: Na+/H+-exchanger 3-based proton secretion leads to CO2 tolerance in cephalopod embryos

Lee

et al. 2013

Front Zool

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BackgroundRegulation of pH homeostasis is a central feature of all animals to cope with acid–base disturbances caused by respiratory CO2. Although a large body of knowledge is available for vertebrate and mammalian pH regulatory systems, the mechanisms of pH regulation in marine invertebrates remain largely unexplored.ResultsWe used squid (Sepioteuthis lessoniana), which are known as powerful acid–base regulators to investigate the pH regulatory machinery with a special focus on proton secretion pathways during environmental hypercapnia. We cloned a Rhesus protein (slRhP), V-type H+-ATPase (slVHA) and the Na+/H+ exchanger 3 (slNHE3) from S. lessoniana, which are hypothesized to represent key players in proton secretion pathways among different animal taxa. Specifically designed antibodies for S. lessoniana demonstrated the sub-cellular localization of NKA, VHA (basolateral) and NHE3 (apical) in epidermal ionocytes of early life stages. Gene expression analyses demonstrated that slNHE3, slVHA and slRhP are up regulated in response to environmental hypercapnia (pH 7.31; 0.46 kPa pCO2) in body and yolk tissues compared to control conditions (pH 8.1; 0.045 kPa pCO2). This observation is supported by H+ selective electrode measurements, which detected increased proton gradients in CO2 treated embryos. This compensatory proton secretion is EIPA sensitive and thus confirms the central role of NHE based proton secretion in cephalopods.ConclusionThe present work shows that in convergence to teleosts and mammalian pH regulatory systems, cephalopod early life stages have evolved a unique acid–base regulatory machinery located in epidermal ionocytes. Using cephalopod molluscs as an invertebrate model this work provides important insights regarding the unifying evolutionary principles of pH regulation in different animal taxa that enables them to cope with CO2 induced acid–base disturbances.

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“…Alternatively, the basolateral entry of ammonia can be facilitated through NH 3 channels of the Rh-glycoprotein family that allow the entry and subsequent hydration of NH 3 to form the ammonium ion in the cytosol. At the apical membrane export of ammonia has been proposed to be facilitated through apical ammonia (NH 3 ) channels in combination with Na + /H + -exchanger (NHE) or proton pump-based [e.g., V-type H + -ATPase (VHA), H + /K + -ATPase] H + extrusion mechanisms that lead to an acid trapping of NH 3 that has been excreted through the NH 3 channels, in the outer boundary layer of excretory epithelia (Wright and Wood, 2009; Gruswitz et al, 2010; Nawata et al, 2010; Wu et al, 2010). The removal of the proton from the ammonium ion at the apical membrane is potentially facilitated by the deprotonating activity found in NH 3 channel proteins (Javelle et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Perfused Gills Reveal Fundamental Principles of pH Regulation and Ammonia Homeostasis in the Cephalopod Octopus vulgaris

Sung

Guh

et al. 2017

Front. Physiol.

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In contrast to terrestrial animals most aquatic species can be characterized by relatively higher blood NH4+ concentrations despite its potential toxicity to the central nervous system. Although many aquatic species excrete NH4+ via specialized epithelia little information is available regarding the mechanistic basis for NH3/NH4+ homeostasis in molluscs. Using perfused gills of Octopus vulgaris we studied acid-base regulation and ammonia excretion pathways in this cephalopod species. The octopus gill is capable of regulating ammonia (NH3/NH4+) homeostasis by the accumulation of ammonia at low blood levels (<260 μM) and secretion at blood ammonia concentrations exceeding in vivo levels of 300 μM. NH4+ transport is sensitive to the adenylyl cyclase inhibitor KH7 indicating that this process is mediated through cAMP-dependent pathways. The perfused octopus gill has substantial pH regulatory abilities during an acidosis, accompanied by an increased secretion of NH4+. Immunohistochemical and qPCR analyses revealed tissue specific expression and localization of Na+/K+-ATPase, V-type H+-ATPase, Na+/H+-exchanger 3, and Rhesus protein in the gill. Using the octopus gill as a molluscan model, our results highlight the coupling of acid-base regulation and nitrogen excretion, which may represent a conserved pH regulatory mechanism across many marine taxa.

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Rh glycoprotein expression is modulated in pufferfish (Takifugu rubripes) during high environmental ammonia exposure

Cited by 97 publications

References 74 publications

Carbon dioxide induced plasticity of branchial acid-base pathways in an estuarine teleost

Carbon dioxide induced plasticity of branchial acid-base pathways in an estuarine teleost

Development in a naturally acidified environment: Na+/H+-exchanger 3-based proton secretion leads to CO2 tolerance in cephalopod embryos

Perfused Gills Reveal Fundamental Principles of pH Regulation and Ammonia Homeostasis in the Cephalopod Octopus vulgaris

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